Molecular pathways involved in the amelioration of myocardial injury in diabetic rats by Kaempferol

International Journal of Molecular Sciences

Volumn 18, Issue 5, 2017, Pages

  Suchal, Kapil ^a   Malik, Salma ^a   Khan, Sana Irfan ^a   Malhotra, Rajiv Kumar ^a   Goyal, Sameer N ^b   Bhatia, Jagriti ^a   Ojha, Shreesh ^c   Arya, Dharamvir Singh ^a  

^a ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

^b R C PATEL INSTITUTE OF PHARMACEUTICAL EDUCATION AND RESEARCH   (India)

^c UNITED ARAB EMIRATES UNIVERSITY   (United Arab Emirates)

Author keywords

AGE RAGE; Apoptosis; Diabetes; Inflammation; Ischemia reperfusion; Kaempferol

Indexed keywords

ADVANCED GLYCATION END PRODUCT; DNA NUCLEOTIDYLEXOTRANSFERASE; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; KAEMPFEROL; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN BAX; PROTEIN BCL 2; STRESS ACTIVATED PROTEIN KINASE 1; TUMOR NECROSIS FACTOR; ADVANCED GLYCATION END PRODUCT RECEPTOR; AGER PROTEIN, RAT; CASPASE 3; KAEMPFEROL DERIVATIVE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; CORONARY REPERFUSION; DIABETES MELLITUS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; GENE INACTIVATION; HEART FUNCTION; HEMODYNAMICS; HYPERGLYCEMIA; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LEFT ANTERIOR DESCENDING CORONARY ARTERY; MALE; MORTALITY RATE; MYOCARDIAL ISCHEMIA REPERFUSION INJURY; NONHUMAN; OXIDATIVE STRESS; POLYACRYLAMIDE GEL ELECTROPHORESIS; RAT; TUNEL ASSAY; WESTERN BLOTTING; ANIMAL; COMPLICATION; CORONARY BLOOD VESSEL; DIET THERAPY; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; GENETICS; HUMAN; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CASPASE 3; CORONARY VESSELS; DIABETES MELLITUS, EXPERIMENTAL; GLYCATION END PRODUCTS, ADVANCED; HUMANS; HYPERGLYCEMIA; INFLAMMATION; INTERLEUKIN-6; KAEMPFEROLS; MAP KINASE KINASE 1; MYOCARDIAL REPERFUSION INJURY; OXIDATIVE STRESS; RATS; RECEPTOR FOR ADVANCED GLYCATION END PRODUCTS; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85019561070     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms18051001     Document Type: Article

References (55)

1. Haffner, S.M.; Lehto, S.; Ronnemaa, T.; Pyorala, K.; Laakso, M. Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N. Engl. J. Med. 1998, 339, 229–234.[CrossRef] [PubMed]
2. Alegria, J.R.; Mille, T.D.; Gibbons, R.J.; Yi, Q.L.; Yusuf, S. Infarct size, ejection fraction, and mortality in diabetic patients with acute myocardial infarction treated with thrombolytic therapy. Am. Heart J. 2007, 154, 743–750.[CrossRef] [PubMed]
3. Fraser, D.A.; Hansen, K.F. Making sense of advanced glycation end products and their relevance to diabetic complications. Inter. Diabetes Monit. 2005, 17, 1–7.
4. Brownlee, M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001, 414, 813–820.[CrossRef] [PubMed]
5. Kass, D.A. Getting better without AGE: New insights into the diabetic heart. Circ. Res. 2003, 92, 704–706.[CrossRef] [PubMed]
6. Candido, R.; Forbes, J.M.; Thomas, M.C.; Thallas, V.; Dean, R.G.; Burns, W.C.; Tikellis, C.; Ritchie, R.H.; Twigg, S.M.; Cooper, M.E. et al. A breaker of advanced glycation end products attenuates diabetes-induced myocardial structural changes. Circ. Res. 2003, 92, 785–792.[CrossRef] [PubMed]
7. Yan, S.F.; Ramasamy, R.; Schmidt, A.M. The RAGE axis: A fundamental mechanism signaling danger to the vulnerable vasculature. Circ. Res. 2010, 106, 842–853.[CrossRef] [PubMed]
8. Bucciarelli, L.G.; Ananthakrishnan, R.; Hwang, Y.C.; Kaneko, M.; Song, F.; Sell, D.R.; Strauch, C.; Monnier, V.M.; Yan, S.F.; Schmidt, A.M. et al. RAGE and modulation of ischemic injury in the diabetic myocardium. Diabetes 2008, 57, 1941–1951.[CrossRef] [PubMed]
9. Soro-Paavonen, A.; Watson, A.M.; Li, J.; Paavonen, K.; Koitka, A.; Calkin, A.C.; Barit, D.; Coughlan, M.T.; Drew, B.G.; Lancaster, G.I. et al. Receptor for advanced glycation end products (RAGE) deficiency attenuates the development of atherosclerosis in diabetes. Diabetes 2008, 57, 2461–2469.[CrossRef] [PubMed]
10. Tikellis, C.; Thomas, M.C.; Harcourt, B.E.; Coughlan, M.T.; Pete, J.; Bialkowski, K.; Tan, A.; Bierhaus, A.; Cooper, M.E.; Forbes, J.M. Cardiac inflammation associated with a Western diet is mediated via activation of RAGE by AGEs. Am. J. Physiol. Endocrinol. Metab. 2008, 295, E323–E330.[CrossRef] [PubMed]
11. Herlaar, E.; Brown, Z. P38 MAPK signalling cascades in inflammatory disease. Mol. Med. Today 1999, 5, 439–447.[CrossRef]
12. Rajesh, M.; Bátkai, S.; Kechrid, M.; Mukhopadhyay, P.; Lee, W.S.; Horváth, B.; Holovac, E.; Cinar, R.; Liaudet, L.; Macki, K. et al. Cannabinoid 1 receptor promotes cardiac dysfunction, oxidative stress, inflammation, and fibrosis in diabetic cardiomyopathy. Diabetes 2012, 61, 716–727.[CrossRef] [PubMed]
13. Wojdyo, A.; Oszmianski, J.; Czemerys, R. Antioxidant activity and phenolic compounds in 32 selected herbs. Food Chem. 2007, 105, 940–949.[CrossRef]
14. Somerset, S.M.; Johannot, L. Dietary flavonoid sources in Australian adults. Nutr. Cancer 2008, 60, 442–449.[CrossRef] [PubMed]
15. Calderón-Montaño, J.M.; Burgos-Morón, E.; Pérez-Guerrero, C.; López-Lázaro, M. A review on the dietary flavonoid kaempferol. Mini-Rev. Med. Chem. 2011, 11, 298–344.[CrossRef] [PubMed]
16. Al-Numair, K.S.; Veeramani, C.; Alsaif, M.A.; Chandramohan, G. Influence of kaempferol, a flavonoid compound, on membrane-bound ATPases in streptozotocin-induced diabetic rats. Pharm. Biol. 2015, 53, 1372–1378.[CrossRef] [PubMed]
17. Yoon, H.Y.; Lee, E.G.; Lee, H.; Cho, I.J.; Choi, Y.J.; Sung, M.S.; Yoo, H.G.; Yoo, W.H. Kaempferol inhibits IL-1β-induced proliferation of rheumatoid arthritis synovial fibroblasts and the production of COX-2, PGE2 and MMPs. Int. J. Mol. Med. 2013, 32, 971–977. [PubMed]
18. Xiao, J.; Sun, G.B.; Sun, B.; Wu, Y.; He, L.; Wang, X.; Chen, R.C.; Cao, L.; Ren, X.Y.; Sun, X.B. Kaempferol protects against doxorubicin-induced cardiotoxicity in vivo and in vitro. Toxicology 2012, 292, 53–62.[CrossRef] [PubMed]
19. Alkhalidy, H.; Moore, W.; Zhang, Y.; McMillan, R.; Wang, A.; Ali, M.; Suh, K.S.; Zhen, W.; Cheng, Z.; Jia, Z. et al. Small molecule kaempferol promotes insulin sensitivity and preserved pancreatic β-cell mass in middle-aged obese diabetic mice. J. Diabetes Res. 2015, 2015, 532984.[CrossRef] [PubMed]
20. Centers for Disease Control and Prevention. National diabetes fact sheet, 2011; U.S. Department of Health and Human Services: Atlanta, GA, USA, 2011. Available online: http://www.diabetesincontrol.com/wpcontent/uploads/PDF/ndep_diabetes_facts_2011.pdf (accessed on 10 April 2017).
21. Centers for Disease Control and Prevention. National Diabetes Statistics Report: Estimates of Diabetes and Its Burden in the United States, 2014; U.S. Department of Health and Human Services: Atlanta, GA, USA, 2014. Available online: https://www.cdc.gov/diabetes/pubs/statsreport14/national-diabetes-report-web.pdf (accessed on 10 April 2017).
22. Rivellese, A.A.; Riccardi, G.; Vaccaro, O. Cardiovascular risk inwomenwith diabetes. Nutr. Metab. Cardiovasc. Dis. 2010, 20, 474–480.[CrossRef] [PubMed]
23. Yang, E.J.; Kim, G.S.; Jun, M.; Song, K.S. Kaempferol attenuates the glutamate-induced oxidative stress in mouse-derived hippocampal neuronal HT22 cells. Food Funct. 2014, 5, 1395–1402.[CrossRef] [PubMed]
24. Ma, H.; Li, S.Y.; Xu, P.; Babcock, S.A.; Dolence, E.K.; Brownlee, M.; Li, J.; Ren, J. Advanced glycation endproduct (AGE) accumulation and AGE receptor (RAGE) up-regulation contribute to the onset of diabetic cardiomyopathy. J. Cell. Mol. Med. 2009, 13, 1751–1764.[CrossRef] [PubMed]
25. Zong, H.; Ward, M.; Madden, A.; Yong, P.H.; Limb, G.A.; Curtis, T.M.; Stitt, A.W. Hyperglycaemia-induced pro-inflammatory responses by retinal Müller glia are regulated by the receptor for advanced glycation end-products (RAGE). Diabetologia 2010, 53, 2656–2666.[CrossRef] [PubMed]
26. El-Mesallamy, H.O.; Hamdy, N.M.; Ezzat, O.A.; Reda, A.M. Levels of soluble advanced glycation end product-receptors and other soluble serum markers as indicators of diabetic neuropathy in the foot. J. Investig. Med. 2011, 59, 1233–1238.[CrossRef] [PubMed]
27. Ojima, A.; Ishibashi, Y.; Matsui, T.; Maeda, S.; Nishino, Y.; Takeuchi, M.; Fukami, K.; Yamagishi, S. Glucagon-like peptide-1 receptor agonist inhibits asymmetric dimethylarginine generation in the kidney of streptozotocin-induced diabetic rats by blocking advanced glycation end product-induced protein arginine methyltranferase-1 expression. Am. J. Pathol. 2013, 182, 132–141.[CrossRef] [PubMed]
28. Zhang, Y.; Liu, D. Flavonol kaempferol improves chronic hyperglycemia-impaired pancreatic β-cell viability and insulin secretory function. Eur. J. Pharmacol. 2011, 670, 325–332.[CrossRef] [PubMed]
29. Luo, C.; Yang, H.; Tang, C.; Yao, G.; Kong, L.; He, H.; Zhou, Y. Kaempferol alleviates insulin resistance via hepatic IKK/NF-κB signal in type 2 diabetic rats. Int. Immunopharmacol. 2015, 28, 744–750.[CrossRef] [PubMed]
30. Yan, S.D.; Schmidt, A.M.; Anderson, G.M.; Zhang, J.; Brett, J.; Zou, Y.S.; Pinsky, D.; Stern, D. Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J. Biol. Chem. 1994, 269, 9889–9897. [PubMed]
31. Coughlan, M.T.; Thorburn, D.R.; Penfold, S.A.; Laskowski, A.; Harcourt, B.E.; Sourris, K.C.; Tan, A.L.; Fukami, K.; Thallas-Bonke, V.; Nawroth, P.P. et al. RAGE-induced cytosolic ROS promote mitochondrial superoxide generation in diabetes. J. Am. Soc. Nephrol. 2009, 20, 742–752.[CrossRef] [PubMed]
32. Loor, G.; Kondapalli, J.; Iwase, H.; Chandel, N.S.; Waypa, G.B.; Guzy, R.D.; Vanden Hoek, T.L.; Schumacker, P.T. Mitochondrial oxidative stress triggers cell death in simulated ischemia-reperfusion. Biochim. Biophys. Acta 2011, 1813, 1382–1394.[CrossRef] [PubMed]
33. Saw, C.L.; Guo, Y.; Yang, A.Y.; Paredes-Gonzalez, X.; Ramirez, C.; Pung, D.; Kong, A.N. The berry constituents quercetin, kaempferol, and pterostilbene synergistically attenuate reactive oxygen species: Involvement of the Nrf2-ARE signaling pathway. Food Chem. Toxicol. 2014, 72, 303–311.[CrossRef] [PubMed]
34. Zhou, M.; Ren, H.; Han, J.; Wang, W.; Zheng, Q.; Wang, D. Protective effects of kaempferol against myocardial ischemia/reperfusion injury in isolated rat heart via antioxidant activity and inhibition of glycogen synthase kinase-3β. Oxid. Med. Cell Longev. 2015, 2015, 481405.[CrossRef] [PubMed]
35. Zeng, S.; Feirt, N.; Goldstein, M.; Guarrera, J.; Ippagunta, N.; Ekong, U.; Dun, H.; Lu, Y.; Qu, W.; Schmidt, A.M. et al. Blockade of receptor for advanced glycation end product (RAGE) attenuates ischemia and reperfusion injury to the liver in mice. Hepatology 2004, 39, 422–432.[CrossRef] [PubMed]
36. Dahlmann, M.; Okhrimenko, A.; Marcinkowski, P.; Osterland, M.; Herrmann, P.; Smith, J.; Heizmann, C.W.; Schlag, P.M.; Stein, U. RAGE mediates S100A4-induced cell motility via MAPK/ERK and hypoxia signaling and is a prognostic biomarker for human colorectal cancer metastasis. Oncotarget 2014, 5, 3220–3233.[CrossRef] [PubMed]
37. Su, B.; Karin, M. Mitogen-activated protein kinase cascades and regulation of gene expression. Curr. Opin. Immunol. 1996, 8, 402–411.[CrossRef]
38. Boulton, T.G.; Nye, S.H.; Robbins, D.J.; Ip, N.Y.; Radziejewska, E.; Morgenbesser, S.D.; DePinho, R.A.; Panayotatos, N.; Cobb, M.H.; Yancopoulos, G.D. ERKs: A family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell 1991, 65, 663–675.[CrossRef]
39. Wang, H.; Zhu, Q.W.; Ye, P.; Li, Z.B.; Li, Y.; Cao, Z.L.; Shen, L. Pioglitazone attenuates myocardial ischemia-reperfusion injury via up-regulation of ERK and COX-2. Biosci. Trends 2012, 6, 325–332.[CrossRef] [PubMed]
40. Gao, X.F.; Zhou, Y.; Wang, D.Y.; Lew, K.S.; Richards, A.M.; Wang, P. Urocortin-2 suppression of p38-MAPK signaling as an additional mechanism for ischemic cardioprotection. Mol. Cell. Biochem. 2015, 398, 135–146.[CrossRef] [PubMed]
41. Kyriakis, J.M.; Avruch, J. Sounding the alarm: Protein kinase cascades activated by stress and inflammation. J. Biol. Chem. 1996, 271, 24313–24316.[CrossRef] [PubMed]
42. Mizukami, Y.; Yoshioka, K.; Morimoto, S.; Yoshida, K. A novel mechanism of JNK1 activation. Nuclear translocation and activation of JNK1 during ischemia and reperfusion. J. Biol. Chem. 1997, 272, 16657–16662.[CrossRef] [PubMed]
43. Yu, D.; Li, M.; Tian, Y.; Liu, J.; Shang, J. Luteolin inhibits ROS-activated MAPK pathway in myocardial ischemia/reperfusion injury. Life Sci. 2015, 122, 15–25.[CrossRef] [PubMed]
44. Li, C.; He, J.; Gao, Y.; Xing, Y.; Hou, J.; Tian, J. Preventive effect of total flavones of Choerospondias axillaries on ischemia/reperfusion-induced myocardial infarction-related MAPK signaling pathway. Cardiovasc. Toxicol. 2014, 14, 145–152.[CrossRef] [PubMed]
45. Shi, L.; Yu, X.; Yang, H.; Wu, X. Advanced glycation end products induce human corneal epithelial cells apoptosis through generation of reactive oxygen species and activation of JNK and p38 MAPK pathways. PLoS ONE 2013, 8, e66781.[CrossRef] [PubMed]
46. Ma, C.; Zhang, Y.; Li, Y.Q.; Chen, C.; Cai, W.; Zeng, Y.L. The role of PPAR in advanced glycation end products-induced inflammatory response in human chondrocytes. PLoS ONE 2015, 10, e0125776.[CrossRef] [PubMed]
47. Liang, Y.; Hou, C.; Kong, J.; Wen, H.; Zheng, X.; Wu, L.; Huang, H.; Chen, Y. HMGB1 binding to receptor for advanced glycation end products enhances inflammatory responses of human bronchial epithelial cells by activating p38 MAPK and ERK1/2. Mol. Cell. Biochem. 2015, 405, 63–71.[CrossRef] [PubMed]
48. Tesch, G.H.; Allen, T.J. Rodent models of streptozotocin-induced diabetic nephropathy. Nephrology 2007, 12, 261–266.[CrossRef] [PubMed]
49. Suchal, K.; Malik, S.; Gamad, N.; Malhotra, R.K.; Goyal, S.N.; Bhatia, J.; Arya, D.S. Kampeferol protects against oxidative stress and apoptotic damage in experimental model of isoproterenol-induced cardiac toxicity in rats. Phytomedicine 2016, 23, 1401–1408.[CrossRef] [PubMed]
50. Suchal, K.; Malik, S.; Gamad, N.; Malhotra, R.K.; Goyal, S.N.; Chaudhary, U.; Bhatia, J.; Ojha, S.; Arya, D.S. Kaempferol attenuates myocardial ischemic injury via Inhibition of MAPK signaling pathway in experimental model of myocardial ischemia-reperfusion injury. Oxid. Med. Cell. Longev. 2016, 2016, 7580731.[CrossRef] [PubMed]
51. Ohkawa, H.; Ohishi, N.; Yagi, K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 1979, 95, 351–358.[CrossRef]
52. Moron, M.S.; Depierre, J.W.; Mannervik, B. Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. Biochim. Biophys. Acta 1979, 582, 67–78.[CrossRef]
53. Marklund, S.; Marklund, G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem. 1974, 47, 469–474.[CrossRef] [PubMed]
54. Aebi, H. Catalase in vitro. Methods Enzymol. 1984, 105, 121–126.[PubMed]
55. Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248–254.[CrossRef]